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Changes in Prolactin in Peripheral Plasma During Lactation in the Brushtail Possum Trichosurus Vulpecula

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Changes in Prolactin in Peripheral Plasma During Lactation in the Brushtail Possum Trichosurus Vulpecula Aust. J. Bioi. Sci., 1986, 39, 171-8 Changes in Prolactin in Peripheral Plasma during Lactation in the Brushtail Possum Trichosurus vulpecula L. A. HindsA and P. A. JanssensB A Division of Wildlife and Rangelands Research, CSIRO, P.O. Box 84, Lyneham, A.C.T. 2602. B Department of Zoology, Australian National University, P.O. Box 4, Canberra, A.C.T. 2601. Abstract A heterologous double-antibody radioimmunoassay has been validated for prolactin in plasma and pituitary preparations of T. vulpecula. Serial dilutions of crude pituitary homogenates and plasmas from several marsupials and purified prolactin from the tammar, Macropus eugenii, showed parallel dose response curves. In both male and female possums plasma prolactin concentrations increased in response to a single intravenous injection of thyrotrophin releasing hormone. Plasma prolactin concentrations were measured in six lactating females (June-November) and in four non-lactating females (July-October). In the following year prolactin levels were also measured in II possums with young less than 50 days old and in 24 possums with young aged between 100 and 145 days. In early lactation prolactin concentrations were low ( < 8 ng/ml) but increased to high levels (> 30 ng/ml) by 120 days and remained high until about 160 days of lactation. Thereafter concentrations declined although the young continued to take milk from the mother for a further 30-50 days. The changes in plasma prolactin concentrations throughout lactation are very similar to those described for the tammar, and this unusual pattern appears to be common to marsupials. Non-lactating possums showed no consistent changes in plasma prolactin concentrations between July and October. Introduction The common brushtail possum, Trichosurus vulpecula (Kerr), (Phalangeridae), an arboreal nocturnal marsupial, is abundant in Australia as well as in New Zealand where it has been introduced. The seasonally breeding female possum is monovular and polyoestrous, the gestation period occupying about 17· 5 days of the 26-day oestrous cycle (Pilton and Sharman 1962). Most young are born between April and June, although a second, minor breeding season occurs between September and November. Thus it is possible for a female to raise two young to independence each year (Dunnet 1956; Smith et al. 1969). Possum young remain associated with their mother for about 200 days. Between birth and 120 days they are found exclusively in the pouch, while after this time they cling to the mother's back (Dunnet 1956; Smith et al. 1969). Weaning is thought to commence at about 130 days and lactation has ceased in most females by 230 days (Smith et al. 1969). The adult possum is primarily a folivore and feeds on a wide range of natural and introduced tree species but it may also eat blossom and fruit, as well as grasses (Hume 1982). During lactation there are marked changes in milk composition (Gross and Bolliger 1959), as well as a large increase in the weight of the sucked mammary gland after 80 days (Smith et al. 1969). Similar changes in milk composition, mammary gland weight and development of the young occur during lactation in the herbivorous tammar, Macropus eugenii (Macropodidae) (Green et al. 1980, 1983; Tyndale-Biscoe 0004-9417/86/020171$02.00 172 L. A. Hinds and P. A. Janssens et al. 1984). Furthermore, in the tammar, there are marked changes in plasma prolactin concentrations during lactation with highest levels occurring, not in early lactation as in eutherians (Cowie et al. 1980), but later in lactation coincident with the increase in mammary gland weight, change-over in milk composition and achievement of homeostasis by the young (Hinds and Tyndale-Biscoe 1982, 1985). Therefore it was of considerable interest to determine whether the unusual pattern of plasma prolactin seen in the lactating tammar is a normal feature of lactation common to marsupials. The possum, which is primarily an arboreal folivore, was a suitable species in which to examine this initially since it is a representative of a different family and displays a different life history strategy from the tammar, which is a terrestrial grazer. Materials and Methods Animals Possums (I. 8-2' 8 kg) were obtained either from the grounds of suburban homes in Canberra or from nearby farming properties. They were captured using cage traps baited with apple and/or aniseed solution and housed in large pens (5 by 3 by 3 m) which contained nest boxes and suspended sacks for shelter. Their diet comprised fresh fruit and vegetables, bread and various types of eucalypt leaves. Water was available ad libitum. At capture the young of five lactating females were weighed and measurements of head and pes length taken. Using the growth curves of Lyne and Verhagen (1957) the ages of these young were estimated to be 46, 72, 90, 117 and 129 days. The actual date of birth of a sixth young born in captivity was known. In the following year the stage of lactation of another 35 possums being used in a different study was determined similarly. Eleven of these possums had young aged between 22 and 50 days, while 24 carried young aged between 100 and 145 days. Collection of Blood Samples To determine whether the assay would measure changes in prolactin levels in vivo, heparinized blood samples (0' 8 ml) were collected at frequent intervals via jugular catheters, inserted as described by Khin Aye Than and McDonald (1973), from two intact male and four intact female possums from 60 min before until 200 min after intravenous injection of thyrotrophin releasing hormone (TRH, Roche Australia, 20 Ilg). Heparinized samples (0, 8 ml) were also collected twice weekly from a lateral tail vein of six lactating females from the time of capture until weaning. Four non-lactating possums were sampled twice weekly from July to October. Two of these animals had not produced a young between May and June while the breeding history of the remaining two females was unknown. In the following year 35 lactating possums with young of various ages were sampled once at the time of capture. After collection blood samples were stored on ice and separated by centrifugation within 30 min. Plasmas were held at - 20°C until assayed for prolactin. Prolactin Assay Assays for prolactin in possum plasma were carried out by a double-antibody procedure, as described previously for the tam mar by Hinds and Tyndale-Biscoe (1982), using antiserum 33/1-8 raised in guinea pigs against human prolactin, and ovine prolactin (NIH-P-SI2) as the standard. Duplicate samples of 100 III plasma were assayed. The accuracy of the assay was determined by the measurement of known amounts of ovine prolactin standard (NIH-P-SI2) added to possum plasma containing endogenous prolactin. The precision of the assay expressed as the intra- and interassay coefficients of variation was assessed by the repeated assay of two pools of possum plasma both within and between assays. To assess the specificity of the assay for marsupial prolactin, various pituitary homogenates and purified pituitary fractions from different species of marsupial were assayed. Adenohypophyses were collected within 15 min of death from T. vulpecula, M. eugenii, eastern quoll (Dasyurus viverrinus) and kowari (Dasyuroides byrnel), stored at - 20°C and crude aqueous homogenates prepared prior to assay. Each anterior pituitary was homogenized in I ml assay buffer, serial dilutions (I : 1000 to I : 512000) prepared and duplicates of 100 III of each dilution tested in the assay. Dilutions of a purified tammar prolactin fraction [74·9(3)Fr.3) prepared by Dr J. Hawkins using the ammonium sulfate fractionation method of Neill and Reichert (1971) were also assayed. To demonstrate parallelism of immunoreactivity between standard ovine prolactin Plasma Prolactin in Possums 173 and endogenous prolactin in plasma, serial dilutions (10-200 1'1) of plasmas from four possums and two tammars were tested. Results Specificity of the Heterologous Assay for Possum and Tammar Prolactin Tracer 125I-Iabelled ovine prolactin bound to antiserum 33/1-8 was displaced in a parallel manner by dilutions of crude pituitary homogenates of all species examined (possum, tammar, eastern quoll, kowari) and by purified tammar prolactin [74·9(3)Fr.3] (Fig. 1). Parallel dose response curves were obtained for serial dilutions Dilutions of pituitary homogena tes (x 1 0 3) 1:64 1:8 1:1 100 1:512 I I x "'- ,,0 • "- 80 ." ""-"'" 0 • ~,,~ "<\"\ '\0 \ 0 co 60 CD C Q) \\0\ \ \ ~ Q) a.. 40 \'\:\\\ \ 20 '\~ \.""'- ..........."" ,,'" .......... 0_0. """ • v""""-.." 0 0.1 1.56 6.25 Ovine prolactin (ng NIH-P-S 12/mIJ Fig. 1. Inhibition curves for prolactin (semi-log plots, percentage B/Bo) of dilutions of aqueous homogenates of anterior pituitaries of tam mar (A), brushtail possum (\7), eastern quoll (_) and kowari (0); of purified wallaby prolactin [74·9(3)Fr.3] (e); and of ovine prolactin (NIH-P-SI2) (x) with antiserum 33/1-8 (I : 36000). of plasmas from an adult male, non-lactating female and lactating female possum and a lactating tammar. No significant displacement of the tracer from the antiserum was induced by plasma from an hypophysectomized female of either species (Fig. 2). Under routine conditions with the antibody dilution fixed at 1 : 36000 (final dilution) the assay was sensitive to 2 ng/ml plasma, being equivalent to the first significant displacement from zero. The recovery of ovine prolactin added to a normal possum plasma in which prolactin was not detectable was closely correlated with the amount added (y = 0'969x - 0'017, r = 0'996, P < 0'001; n = 24) and intra-assay coefficients of variation determined from replicate assays from two pools of possum plasma containing 8· 5 and 32· 5 ng/ml were 10· 0 and 6· 5% respectively (n = 10 for each pool).
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